Polyploidy on Islands: Its Emergence and Importance for Diversification
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ORIGINAL RESEARCH published: 04 March 2021 doi: 10.3389/fpls.2021.637214 Polyploidy on Islands: Its Emergence and Importance for Diversification Heidi M. Meudt 1*, Dirk C. Albach 2, Andrew J. Tanentzap 3, Javier Igea 3, Sophie C. Newmarch 4, Angela J. Brandt 5, William G. Lee 5 and Jennifer A. Tate 4* 1 Museum of New Zealand Te Papa Tongarewa, Wellington, New Zealand, 2 Institute of Biology and Environmental Sciences, University of Oldenburg, Oldenburg, Germany, 3 Ecosystems and Global Change Group, Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom, 4 School of Fundamental Sciences, Massey University, Palmerston North, New Zealand, 5 Manaaki Whenua – Landcare Research, Dunedin, New Zealand Edited by: Whole genome duplication or polyploidy is widespread among floras globally, but Natascha D. Wagner, traditionally has been thought to have played a minor role in the evolution of island University of Göttingen, biodiversity, based on the low proportion of polyploid taxa present. We investigate five Germany island systems (Juan Fernández, Galápagos, Canary Islands, Hawaiian Islands, and Reviewed by: Daniel Crawford, New Zealand) to test whether polyploidy (i) enhances or hinders diversification on islands University of Kansas, and (ii) is an intrinsic feature of a lineage or an attribute that emerges in island environments. United States Marc S. Appelhans, These island systems are diverse in their origins, geographic and latitudinal distributions, Georg-August-University levels of plant species endemism (37% in the Galapagos to 88% in the Hawaiian Islands), Goettingen, Germany and ploidy levels, and taken together are representative of islands more generally. *Correspondence: We compiled data for vascular plants and summarized information for each genus on Heidi M. Meudt [email protected] each island system, including the total number of species (native and endemic), generic Jennifer A. Tate endemicity, chromosome numbers, genome size, and ploidy levels. Dated phylogenies [email protected] were used to infer lineage age, number of colonization events, and change in ploidy level Specialty section: relative to the non-island sister lineage. Using phylogenetic path analysis, we then tested This article was submitted to how the diversification of endemic lineages varied with the direct and indirect effects of Plant Systematics and Evolution, a section of the journal polyploidy (presence of polyploidy, time on island, polyploidization near colonization, Frontiers in Plant Science colonizer pool size) and other lineage traits not associated with polyploidy (time on island, Received: 03 December 2020 colonizer pool size, repeat colonization). Diploid and tetraploid were the most common Accepted: 11 February 2021 ploidy levels across all islands, with the highest ploidy levels (>8x) recorded for the Canary Published: 04 March 2021 Islands (12x) and New Zealand (20x). Overall, we found that endemic diversification of Citation: Meudt HM, Albach DC, our focal island floras was shaped by polyploidy in many cases and certainly others still Tanentzap AJ, Igea J, Newmarch SC, to be detected considering the lack of data in many lineages. Polyploid speciation on the Brandt AJ, Lee WG and Tate JA (2021) Polyploidy on Islands: islands was enhanced by a larger source of potential congeneric colonists and a change Its Emergence and Importance in ploidy level compared to overseas sister taxa. for Diversification. Front. Plant Sci. 12:637214. Keywords: colonization, diversification, endemism, island floras, ploidy level, phylogenetic path analysis, doi: 10.3389/fpls.2021.637214 polyploidy, whole genome duplication Frontiers in Plant Science | www.frontiersin.org 1 March 2021 | Volume 12 | Article 637214 Meudt et al. Polyploidy on Islands INTRODUCTION phylogenetic context was lacking in previous studies, which is important because the phylogeny will indicate the number Since the time of Darwin (1839), the study of island biotas of origins on the island as well as patterns of diversification has provided major advances that have profoundly influenced on the island related to polyploidy or other factors. ecological, evolutionary, and biogeographical theory (MacArthur As robust (and increasingly, dated) phylogenetic hypotheses and Wilson, 1967; Mayr, 1967; Carlquist, 1974; Emerson, 2002). have amassed over the last several decades, along with continued Island biotas are generally the net outcome of immigration efforts to document chromosome numbers, we now have the (dispersal and establishment), local diversification, and extinction capability to test the role of polyploidy in contributing to (Carlquist, 1974), and these processes are known to be influenced species diversification on islands in a phylogenetic context by specifics of the island, such as age, area, distance from (Kellogg, 2016; Crawford and Archibald, 2017). As species in nearest potential source floras Rosenzweig,( 1995), and local many different island floras are known to have diverse habitat (abiotic and biotic) conditions (Savolainen et al., 2006; chromosome numbers and form species-rich groups, they may Vamosi et al., 2018). Islands may also pose selective filters not be chromosomally static lineages as previously thought that may be apparent in the intrinsic traits of species, including (Soltis et al., 2009; New Zealand: Murray and de Lange, 2011; those increasing their ability to disperse, colonize, and establish Canary Islands: Caujapé-Castells et al., 2017). A recent analysis in novel habitats (Crawford et al., 2009; Vargas et al., 2015). of the global distribution of polyploids indicated polyploid Among those traits, whole genome duplication or polyploidy frequency is highest in temperate areas rich in perennial herbs, has been suggested to be central to facilitating long-distance including mountainous areas (Rice et al., 2019). Analyzed from dispersal (Linder and Barker, 2014), the survival of small a global perspective, several island systems are polyploid-rich, populations (Rodriguez, 1996), and evolution of novel traits including the Hawaiian Islands (50% of analyzed species are (Soltis et al., 2014), all features of many island floras. Polyploids polyploid), New Zealand (46%), and Galápagos Islands (46%), are broadly categorized as autopolyploids, when formed within whereas others have lower polyploid frequencies – such as a species, or allopolyploids, when formed between genetically the Canary Islands (32%) – or insufficient data (Juan Fernández: distinct species (Stebbins, 1947). Polyploidy, especially 0 of 2 species included were polyploid; Rice et al., 2019). allopolyploidy, may also be a mechanism for increasing the However, that study was focused primarily on assessing external genetic diversity of the colonizer (Crawford and Stuessy, 1997; drivers of polyploid plant distribution globally, not on island Carr, 1998), which is often low for island colonizers and lineages systems, and did not utilize dated phylogenies. A dated (e.g., Frankham, 1997; but see García-Verdugo et al., 2015). phylogenetic context allows a more precise determination of Thus, polyploidy could have multiple advantages, particularly when diversification and polyploidization have occurred within in island floras. each lineage (i.e., as separate events), and puts the focus on Despite its potential benefits, polyploidy has been (multiple) lineage ages rather than a single island age. Such historically suggested to play a minor role in diversification an approach can generate multiple independent data points of island floras, with many groups showing “chromosomal that can be analyzed together to address the timing and role stasis” (Carr, 1998; Stuessy and Crawford, 1998). For the of polyploidy on islands. Dated phylogenies are especially oceanic island systems that inform this perspective (Hawaiian, important in the context of island diversification because they Juan Fernández, Galápagos, and Bonin Islands), make it possible to estimate in situ diversification rates and paleopolyploidy was suggested to have helped some lineages to consider in the analyses the geological processes (e.g., volcano establish, with little polyploidization thereafter Carr,( 1998; eruptions, inundations) that may affect lineages at different Stuessy and Crawford, 1998), such as in Gossypium (Malvaceae; evolutionary time scales. Figure 1). Thus, while polyploid, these oceanic island lineages We hypothesize that polyploidy has played an important remained chromosomally static. By contrast, chromosomal role in the diversification of island floras by facilitating dispersal variation was found in two island systems near their continental and establishment of plants to islands, and/or by generating source, the Queen Charlotte Islands and Canary Islands additional diversity through varying ploidy levels. To test a (Stuessy and Crawford, 1998). Although Crawford et al. conceptual model for how polyploidy influences species (2009) began to address the question of the evolution of diversification on islands, we synthesized published chromosome polyploidy in island systems and its role in diversification and divergence time data for 150 lineages representing 1,805 (for Asteraceae; Crawford et al., 2009), others discounted endemic species across the Juan Fernández, Canary, Hawaiian, its impact (Stuessy et al., 2014; Crawford and Archibald, and New Zealand archipelagos (Figure 1). All these island 2017). However, in those studies (Carr, 1998; Stuessy and systems, except New Zealand, have been included